Hair plate

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Hair-plates are a type of proprioceptor found in the folds of insect joints.[1] They consist of a cluster of hairs, in which each hair is innervated by a single mechanosensory neuron. Functionally, hair-plates operate as "limit-detectors" by signaling the extreme ranges of motion of a joint.[2]

Structure and Neuron Anatomy

Fig.1 Schematic cross-section of a hair-plate. Hair-plates are positioned next to folds within the cuticle, so that the deflection of the hairs signal the relative movements of adjoining body segments.

Hair-plates typically consist of a cluster of individual sensory hairs, in which each hair is innervated by a single sensory neuron[1] (Fig. 1). The number of sensory hairs can vary across hair-plates as well as the length of hairs within a hair-plate.[3][4] Hair-plates are often positioned within folds of cuticle, so that hairs are deflected during joint movement.[5] They are located on different body parts, including the legs,[6][7][8][3][9] neck,[10][11] and antennae.[12][13] On the legs of insects, hair-plates are typically found at the proximal joints (i.e. thorax-coxa, coxa-trochanter, and trochanter-femur joints) and may vary in number across the front, middle, and hind legs .

The anatomy of a hair-plate neuron is composed of dendrites that are imbedded within a cuticular hair, an elongated cell body, and an axon that projects into the ventral nerve cord, specifically the intermediate neuropil of the corresponding leg.[14] In the front leg neuropil of Drosophila melanogaster, hair-plate neurons arborize along the ventral surface and send processes dorsally and medially. Moreover, the neurons of the hair-plates located within the coxa-thorax joint project through the ventral, dorsal, and accessory prothoracic nerves, whereas, the hair-plate neurons elsewhere on the leg project through the prothoracic leg nerve.[15][16] The morphology of the arbors of specific hair-plate neurons associated with the middle and hind legs remains unknown, along with what nerves they project through.

Function

Hair-plates function as proprioceptors.[1] The sensory neurons innervating the hair-plate may respond phasically (rapidly adapting) or tonically (slowly adapting) to deflections of the hairs .[9][17] Thus, hair-plates can encode the position and movement of adjoining body segments. The projections of neurons associated with the longer hairs of a hair plate can form direct, mono-synaptic excitatory chemical synapses with motor neurons[3] as well as synapses with interneurons that provide inhibitory input onto motor neurons. Therefore, hair-plates are situated to provide rapid feedback to control the movement of the associated leg. Little is known about the function and synaptic partners of the neurons associated with the smaller hairs. Hair-plate neurons are also involved in the presynaptic inhibition to other proprioceptors.[18]

Role of hair-plates during behavior

Walking

Hair-plates located at the leg joints provide sensory feedback for the control of walking.[6][7][19][2][20][21][22] In stick insects and cockroaches, the surgical removal of coxa hair-plates alters the extremes of leg movement in such a way that the leg may overstep and collide with the anterior leg. This indicates that proprioceptive signals from these hair-plates limit the forward movement of the leg by signaling the end of swing phase.[6][19] This “limit-detector” function is similar to that of mammalian joint receptors.[23] Ablating the anterior trochanteral hair-plate on a stick insect leg did not alter the coordination between legs, but rather resulted in that leg being held higher. The hair-plates on the trochanter appear to control the height of the animal,[24] which is likely important for climbing over obstacles and the recovery of walking after unexpected perturbations to the legs. Therefore, hair-plates located at different joints along the leg may have different functions.

Feeding

The mechanosensory information from hair-plates on the leg also contribute to the regulation of feeding behavior in fruit flies, Drosophila melanogaster. The integration of this mechanosensory information along with olfactory information from antennal neurons control the proboscis extension reflex (PER) in flies. Thus, the sensory input from hair-plates is integrated with the information from other sensory modalities to control behaviors beyond walking.[25]

Posture

Hair-plates located on the neck (known as the prosternal organ) monitor head position relative to the thorax and provide sensory feedback for the control of head posture.[10][11] In the blowfly Calliphora, surgical removal of the prosternal organ hairs on one side causes the fly to compensate by rolling the head toward the operated side.[10] These results suggest that the prosternal organ may be involved in gaze stabilization.

Antennal movement

Hair-plates located on the proximal segments of the antenna (Fig. 2) provide sensory feedback for the control of antennal movement[13] and are thought to play an important role in active sensing, object localization, and targeted reaching movements.[12][26]

Fig. 2 Lateral view of a cockroach antenna, showing the hair plates at the base.

See also

References

  1. ^ a b c Tuthill; Wilson (2016). "Mechanosensation and Adaptive Motor Control in Insects". Current Biology. 26 (20): R1022–R1038. doi:10.1016/j.cub.2016.06.070. PMC 5120761. PMID 27780045.
  2. ^ a b Bässler, U. (1977-06-01). "Sensory control of leg movement in the stick insect Carausius morosus". Biological Cybernetics. 25 (2): 61–72. doi:10.1007/BF00337264. ISSN 1432-0770. PMID 836915. S2CID 2634261.
  3. ^ a b c Pearson; Wong; Fourtner (1976). "Connexions between hair-plate afferents and motorneurones in the cockroach leg". J Exp Biol. 64 (1): 251–266. doi:10.1242/jeb.64.1.251. PMID 5571.
  4. ^ Petryszak, Anna (1994). "External proprioceptors on the legs of insects of higher orders". Acta Biologica Cracoveinsia. 36: 13–22.
  5. ^ Pringle, J. W. S. (1938-10-01). "Proprioception In Insects: III. The Function Of The Hair Sensilla At The Joints". Journal of Experimental Biology. 15 (4): 467–473. doi:10.1242/jeb.15.4.467. ISSN 0022-0949.
  6. ^ a b c Wendler, Gernot (1964-03-01). "Laufen und Stehen der Stabheuschrecke Carausius morosus: Sinnesborstenfelder in den Beingelenken als Glieder von Regelkreisen". Zeitschrift für vergleichende Physiologie (in German). 48 (2): 198–250. doi:10.1007/BF00297860. ISSN 1432-1351. S2CID 37588295.
  7. ^ a b Markl, Hubert (1962-09-01). "Borstenfelder an den Gelenken als Schweresinnesorgane bei Ameisen und anderen Hymenopteren". Zeitschrift für vergleichende Physiologie (in German). 45 (5): 475–569. doi:10.1007/BF00342998. ISSN 1432-1351. S2CID 38336445.
  8. ^ Murphey, R. K.; Possidente, Debra; Pollack, Gerald; Merritt, D. J. (1989). "Modality-specific axonal projections in the CNS of the flies Phormia and Drosophila". Journal of Comparative Neurology. 290 (2): 185–200. doi:10.1002/cne.902900203. ISSN 1096-9861. PMID 2512333. S2CID 6726012.
  9. ^ a b Newland; Watkins; Emptage; Nagayama (1976). "The structure, response properties, and development of a hair plate on the mesothoracic leg of the locust". J Exp Biol. 64: 233–249.
  10. ^ a b c Preuss; Hengstenberg (1992). "Structure and kinematics of the prosternal organs and their influence on head position in the blowfly Calliphora erythocephala". J Comp Physiol. 171: 483–493. doi:10.1007/BF00194581. S2CID 13379331.
  11. ^ a b Paulk; Gilbert (2006). "Proprioceptive encoding of head position in the black soldier fly, Hermetia illucens". J Exp Biol. 209 (Pt 19): 3913–3924. doi:10.1242/jeb.02438. PMID 16985207. S2CID 12169844.
  12. ^ a b Okada; Toh (2000). "The role of antennal hair plates in object-guided tactile orientation of the cockroach". Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology. 186 (9): 849–857. doi:10.1007/s003590000137. PMID 11085638. S2CID 1917793.
  13. ^ a b Krause, André F.; Winkler, Andrea; Dürr, Volker (January 2013). "Central drive and proprioceptive control of antennal movements in the walking stick insect". Journal of Physiology, Paris. 107 (1–2): 116–129. doi:10.1016/j.jphysparis.2012.06.001. ISSN 1769-7115. PMID 22728470. S2CID 11851224.
  14. ^ Merritt, D. J.; Murphey, R. K. (1992-08-01). "Projections of leg proprioceptors within the CNS of the fly Phormia in relation to the generalized insect ganglion". The Journal of Comparative Neurology. 322 (1): 16–34. doi:10.1002/cne.903220103. ISSN 0021-9967. PMID 1430308. S2CID 10317647.
  15. ^ Kuan, Aaron T.; Phelps, Jasper S.; Thomas, Logan A.; Nguyen, Tri M.; Han, Julie; Chen, Chiao-Lin; Azevedo, Anthony W.; Tuthill, John C.; Funke, Jan; Cloetens, Peter; Pacureanu, Alexandra (December 2020). "Dense neuronal reconstruction through X-ray holographic nano-tomography". Nature Neuroscience. 23 (12): 1637–1643. doi:10.1038/s41593-020-0704-9. ISSN 1546-1726. PMC 8354006. PMID 32929244.
  16. ^ Phelps, Jasper S.; Hildebrand, David Grant Colburn; Graham, Brett J.; Kuan, Aaron T.; Thomas, Logan A.; Nguyen, Tri M.; Buhmann, Julia; Azevedo, Anthony W.; Sustar, Anne; Agrawal, Sweta; Liu, Mingguan (2021-02-04). "Reconstruction of motor control circuits in adult Drosophila using automated transmission electron microscopy". Cell. 184 (3): 759–774.e18. doi:10.1016/j.cell.2020.12.013. ISSN 0092-8674. PMC 8312698. PMID 33400916.
  17. ^ French; Wong (1976). "The responses of trochanteral hair plate sensilla in the cockroach to periodic and random displacements". Biol. Cyber. 22: 33–38. doi:10.1007/BF00340230. S2CID 9672599.
  18. ^ Stein; Schmitz (1999). "Multimodal convergence of presynaptic afferent inhibition in insect proprioceptors". Neurophysiology. 82 (1): 512–514. doi:10.1152/jn.1999.82.1.512. PMID 10400981.
  19. ^ a b Wong; Pearson (1976). "Properties of the trochanteral hair plate and its function in the control of walking in the cockroach". J Exp Biol. 64 (1): 233–249. doi:10.1242/jeb.64.1.233. PMID 1270992.
  20. ^ Cruse, H.; Dean, J.; Suilmann, M. (1984-09-01). "The contributions of diverse sense organs to the control of leg movement by a walking insect". Journal of Comparative Physiology A. 154 (5): 695–705. doi:10.1007/BF01350223. ISSN 1432-1351. S2CID 2519441.
  21. ^ Schmitz, J. (1986-10-01). "The depressor trochanteris motoneurones and their role in the coxo-trochanteral feedback loop in the stick insect Carausius morosus". Biological Cybernetics. 55 (1): 25–34. doi:10.1007/BF00363975. ISSN 1432-0770. S2CID 23692174.
  22. ^ Theunissen, Leslie M.; Vikram, Subhashree; Dürr, Volker (2014-09-15). "Spatial co-ordination of foot contacts in unrestrained climbing insects". Journal of Experimental Biology. 217 (18): 3242–3253. doi:10.1242/jeb.108167. ISSN 0022-0949. PMID 25013102.
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  25. ^ Oh, Soo Min; Jeong, Kyunghwa; Seo, Jeong Taeg; Moon, Seok Jun (2021-02-16). "Multisensory interactions regulate feeding behavior in Drosophila". Proceedings of the National Academy of Sciences. 118 (7): e2004523118. Bibcode:2021PNAS..11804523O. doi:10.1073/pnas.2004523118. ISSN 0027-8424. PMC 7896327. PMID 33558226.
  26. ^ Schütz, Christoph; Dürr, Volker (2011-11-12). "Active tactile exploration for adaptive locomotion in the stick insect". Philosophical Transactions of the Royal Society B: Biological Sciences. 366 (1581): 2996–3005. doi:10.1098/rstb.2011.0126. ISSN 0962-8436. PMC 3172591. PMID 21969681.
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